Introduction
The Bolivian Yungas are situated in Endemic Bird Areas 054 and 055 (Bolivian and Peruvian lower and upper Yungas, respectively; Stattersfield et al. Reference Stattersfield, Crosby, Long and Wege1998, www.birdlife.org/action/science/endemic_bird_areas/index.html), both of which are considered of urgent conservation priority, and in the southern part of the Tropical Andes biodiversity and conservation hotspot of Myers et al. (Reference Myers, Mittermeier, Mittermeier, da Fonseca and Kent2000). They extend from about 13°30’ S in depto. La Paz to 18°00’ S in depto. Santa Cruz and reach from Andean foothills (c. 500 m altitude) up to isolated Polylepis forest patches (to c. 4,200 m) above the closed timberline. The Yungas ecoregion is Bolivia's top priority for bird conservation (Herzog et al. Reference Herzog, Soria Auza and Hennessey2005b) and contains about 600 (43%) of Bolivia's c. 1,420 bird species (Hennessey et al. Reference Hennessey, Herzog and Sagot2003b, authors’ unpubl. data), including 14 Bolivian endemics and near-endemics, 43 restricted-range species (see Stattersfield et al. Reference Stattersfield, Crosby, Long and Wege1998) and 12 threatened species (see Hennessey et al. Reference Hennessey, Herzog and Sagot2003b).
Up to the early 1990s the majority of ornithological field work in the Yungas and other regions in Bolivia was carried out by collecting expeditions primarily from North American museums, and specimen localities were far and few between. Not surprisingly, many bird species were considered poorly known (e.g., Remsen et al. Reference Remsen, Parker and Ridgely1982, Reference Remsen, Traylor and Parkes1987, Reference Remsen, Schmitt and Schmitt1988; Remsen and Traylor Reference Remsen and Traylor1983; Remsen Reference Remsen1984; Parker et al. Reference Parker, Bates and Cox1992). Over the past 10 to 15 years, however, our knowledge of bird distributions in the Bolivian Yungas has improved considerably (see, e.g., Perry et al. Reference Perry, Kessler and Helme1997, Herzog et al. Reference Herzog, Fjeldså, Kessler and Balderrama1999, Hennessey Reference Hennessey2003a,Reference Hennesseyb, Hennessey et al. Reference Hennessey, Herzog, Kessler and Robison2003a, Hennessey and Gomez Reference Hennessey and Gomez2003, Herzog et al. Reference Herzog, Kessler and Bach2005a, MacLeod et al. Reference MacLeod, Ewing, Herzog, Bryce, Evans and Maccormick2005), allowing for a reassessment of the natural history and conservation status of numerous species once considered poorly known (e.g., Bryce et al. Reference Bryce, Hennessey, MacLeod, Evans, Ewing, Herzog, Maccormick and Gomez2005), including the threatened (BirdLife International 2000, 2004) Yungas endemics Bolivian Recurvebill Simoxenops striatus (Furnariidae) and Yungas Antwren Myrmotherula grisea (Thamnophilidae). Both are currently considered ‘Vulnerable’ under IUCN criteria of small population, predicted population decline and, in the case of Bolivian Recurvebill small extent of occurrence and area of occupancy (BirdLife International 2007a,b).
Bolivian Recurvebill is among the country's most poorly understood bird species. For over 50 years, this species was known from only five specimens, four of which were collected in the 1930s by M. A. Carriker in humid Andean foothill forest (Vaurie Reference Vaurie1980) at Santa Ana on the Río Coroico (670 m), depto. La Paz (Carriker Reference Carriker1935), and at El Palmar (800 m), depto. Cochabamba (Bond and Meyer de Schauensee Reference Bond and Meyer de Schauensee1941). The fifth specimen (housed at the Louisiana State University Museum of Natural Science) was collected in 1954 by F. Steinbach at Alto Palmar (1,100 m) in lower Yungas forest above El Palmar. In 1989, Parker et al. (Reference Parker, Bates and Cox1992) rediscovered the Bolivian Recurvebill at a new locality in the upper Río Saguayo valley (700–800 m) of Amboró National Park, depto. Santa Cruz, providing the first data on the species’ natural history, and in 1992 Whitney et al. (Reference Whitney, Rowlett and Rowlett1994) observed two birds 48 km by road southwest of Villa Tunari (1,080–1,090 m), depto. Cochabamba. Until recently, those were the only known localities for the Bolivian Recurvebill.
Yungas Antwren also was described by Carriker (Reference Carriker1935) based on six specimens from Santa Ana (670 m), depto. La Paz. Two specimens at the Carnegie Museum, collected as early as 1917 at Cerro Hosane, Río Blanco (1,200 m), depto. Santa Cruz, had apparently been overlooked by Carriker (Remsen et al. Reference Remsen, Parker and Ridgely1982). A further specimen was collected in 1937 at El Palmar (800 m), depto. Cochabamba (Collar et al. Reference Collar, Gonzaga, Krabbe, Madroño Nieto, Naranjo, Parker and Wege1992). From 1960 to 1981 an additional six specimens were collected (housed at the Louisiana State University Museum of Natural Science) at four localities in the departments of Santa Cruz (Santa Rita, 500 m), Cochabamba (Alto Palmar, 1,100 m) and La Paz (Serranía Bellavista, 1,550 m; Río Beni 20 km N Puerto Linares, 600 m) (Remsen et al. Reference Remsen, Parker and Ridgely1982), and the species was observed by R. S. Ridgely (Remsen et al. Reference Remsen, Parker and Ridgely1982) north of Caranavi (1,400 m), depto. La Paz, by Parker et al. (Reference Parker, Bates and Cox1992) in the upper Río Saguayo valley (650–1,000 m), depto. Santa Cruz, and by T. A. Parker (Collar et al. Reference Collar, Gonzaga, Krabbe, Madroño Nieto, Naranjo, Parker and Wege1992) in the Serranía Raigones (800 m), depto. Santa Cruz. The only primary literature sources on the natural history of Yungas Antwren are Remsen et al. (Reference Remsen, Parker and Ridgely1982), Parker et al. (Reference Parker, Bates and Cox1992) and Perry et al. (Reference Perry, Kessler and Helme1997), who stressed the participation of the species in mixed-species foraging flocks from the understorey (Remsen et al. Reference Remsen, Parker and Ridgely1982, Perry et al. Reference Perry, Kessler and Helme1997) to the lower canopy (Parker et al. Reference Parker, Bates and Cox1992, Perry et al. Reference Perry, Kessler and Helme1997). Parker et al. (Reference Parker, Bates and Cox1992) stated that “this seemingly rare species is almost unknown in life.” In fact, its loud song was unknown until 1996 when recorded for the first time by SKH (see Mayer Reference Mayer2000, Isler and Whitney Reference Isler and Whitney2002).
Over the past 12 years we obtained new data on the natural history of Bolivian Recurvebill and Yungas Antwren at a number of new localities in the Bolivian Yungas that notably increase their known distributional ranges. We also report on the first records of each species for extreme southeast Peru. Additionally, for the first time we present population density and size estimates for both species in the central portion of their range. In conjunction these data indicate that both species no longer merit threatened status, and that they should be downlisted to ‘Near Threatened’. Our new locality data up to 1999 were included as personal communications in Threatened birds of the world (BirdLife International 2000, 2004), but they are presented formally and in detail herein. Data collected after 1999 are presented here for the first time. Because both species have very similar geographical distributions and often occur syntopically they are treated together rather than in separate publications.
Study areas
Most of the new distributional data presented here were obtained by the authors during rapid assessment surveys at a number of localities throughout the Bolivian Yungas. Coordinates, altitudes and brief notes on habitat for most localities are presented in Table 1 and in the Supplementary materials. Two sites where we obtained important additional data are described in more detail here.
Summary of Bolivian Recurvebill Simoxenops striatus (SIST) and Yungas Antwren Myrmotherula grisea (MYGR) locality data. See text and Supplementary materials for details on locality records. Coordinates and altitudes of literature and specimen localities were verified based on field knowledge of the authors, topographic maps and Google Earth.
1 The coordinates for Río Saguayo given by Parker et al. (Reference Parker, Bates and Cox1992) (17°50’S, 63°39’W) were an error.
2 Paynter (Reference Paynter1992) stated that his identification of this locality was uncertain and gave coordinates for a site in the lowlands c. 15 km north of Buena Vista, which is at an altitude of c. 300 m (not 500 m as given by Remsen et al. Reference Remsen, Parker and Ridgely1982) and falls outside the distributional range of Yungas Antwren. The coordinates given here correspond to a semi-deciduous forest site c. 26 km southwest of Santa Cruz de la Sierra, which matches the altitude given by Remsen et al. (Reference Remsen, Parker and Ridgely1982) and is much more likely to be the actual collecting locality.
Cordillera Mosetenes, a remote mountain range located in the Andean foothill region of depto. Cochabamba, is separated from the main Andes by the Altamachi River. It is about 130 km long, 20–25 km wide (covering c. 3,000 km2), up to 2,050 m high and probably contains the largest completely uninhabited forest tract in Bolivia. It is one of the country's most humid regions and, due to its steep topography, is of extremely difficult access. Parts of the area are formally protected in Isiboro-Sécure Indigenous Territory and National Park. Bird surveys on Cordillera Mosetenes were conducted by SKH in a radius of c. 1 km around a small lagoon (Laguna Carachupa; Table 1) from 28 August to 21 September 2003, with several trails reaching from stream valleys at about 1,200 m altitude to a mountain ridge at 1,600 m. Rather than habitat characteristics, the sole criterion for choosing this site was the availability of an open area where a helicopter could land.
The vegetation at our study site on Cordillera Mosetenes (MK, unpubl. data) can be divided into five main categories. As determined from several over-flights by small airplane and helicopter by the authors, this habitat mosaic stretches across 80–90% of the area of Cordillera Mosetenes. (1) Mature forest was 20–25 m tall, had a rather open understorey and was restricted to scattered patches about 0.1–0.5 ha in extent. Epiphytic plants were present in moderate density and abundant only on scattered, up to 35 m tall emergent trees (Ficus spp.). (2) Most of the area was covered by regenerating forest of variable age, caused by natural disturbances due to landslides or tree falls. Older regenerating forest differed from mature forest in its lower canopy height (10–20 m), lack of thick-trunked trees, denser understorey, and fewer epiphytes. (3) Less widespread young successional stages were dominated by dense scrub (Panicum sp., Solanum spp., Acalypha spp., Hedyosmum spp.), with emergent trees (Cecropia spp.) to 12 m tall. (4) Large tracts were formed by up to 15 m tall Guadua bamboo forest. Within dense bamboo stands very little tree regeneration was observed. (5) Stunted ridge forest occurred at 1,500–1,600 m, with trees 3–12 m tall (exceptionally to 15 m) and thickly covered in liverworts, mosses and vascular epiphytes. Small Chusquea bamboo was frequent, but did not form dense thickets.
Los Volcanes (Table 1) is a private 297 ha reserve immediately adjacent to Amboró National Park, depto. Santa Cruz. It is situated on the transition from the tropical humid Yungas to subtropical inter-Andean dry valleys of southern Bolivia and consists of steep sandstone hills intersected by narrow valleys at altitudes of 1,000–1,350 m. Mean annual precipitation is c. 1,300 mm (Herzog and Kessler Reference Herzog and Kessler2002) and characterized by strong seasonality, with about 80% of the rainfall occurring from October to April (SKH, unpubl. data). Topographical factors lead to a marked differentiation of vegetation types, with drought-deciduous (dry) forest on sunny north-facing slopes, semi-deciduous forest on partly shaded slopes and evergreen forest on valley bottoms and adjacent, mostly shaded slopes. Chusquea bamboo was abundant in all forest types with a flowering and fruiting climax in the rainy season (November to March) 2000/2001, followed immediately afterwards by a complete, area-wide bamboo die-off. In 2003 bamboo began to recover slowly, but by late 2005 it was still patchy and not nearly as abundant as during its previous climax.
Methods
Survey methods
Rapid assessment surveys were audio-visual and relied heavily on the use of sound recording (Parker Reference Parker1991) for species documentation and on playback for the identification of unfamiliar bird voices. Field work at most sites aimed at maximizing survey area, covering a new area on most mornings starting with or before the dawn chorus. We kept track of the number of individuals per species observed either consecutively throughout the entire survey (Herzog et al. Reference Herzog, Kessler and Cahill2002) or in summary form at the end of each survey day (Hennessey and Gomez Reference Hennessey and Gomez2003). Sound recordings of Bolivian Recurvebill made by ABH in 1998 were deposited at the Macaulay Library of Natural Sounds (MLNS), Cornell Laboratory of Ornithology, U.S.A., and are included in Mayer (Reference Mayer2000). Recordings of Yungas Antwren made by SKH in 1996 are included in Mayer (Reference Mayer2000), Schulenberg (Reference Schulenberg2000) and Isler and Whitney (Reference Isler and Whitney2002).
Additional methods were used at two sites. During a rapid assessment expedition on Cordillera Mosetenes, survey duration and relative abundance of both species allowed for the use of time consuming territory mapping with the help of playback of song sound recordings. SKH also conducted 16-minute point counts during the first three morning hours (beginning at dawn) in an attempt to use distance sampling for population density estimation. However, only eight spatially independent (minimum distance 250 m) point count stations could be established along the available survey trails (see below), and a total of 14 counts at those stations resulted in only a single detection each of Bolivian Recurvebill and Yungas Antwren, so point count surveys were not continued. This scarcity of detections probably is at least partly a result of the vocal activity pattern of both species, which vocalize predominantly during the dawn chorus and only very sporadically during the remainder of the morning.
Due to the potential problems of territory mapping with unmarked individuals, the objective was to determine the total number of territories falling into the study area, regardless of whether they were completely contained in the area, rather than estimating the absolute size of each territory. An area of about 20 ha at altitudes of 1,200–1,600 m was surveyed intensively along newly cut trails over a 24-day period in August and September 2003. Dense vegetation and steep topography limited field work to the trail system in most of the survey area. A hand-held GPS unit was used to determine the linear horizontal distance between the origin and terminus (or a major shift in direction) of each trail (transect), ignoring minor curves and switchbacks and topographic complexity of the area. Assuming that vocalizations of both species can be detected up to a distance of 50 m on both sides of a transect (see, e.g., Schieck Reference Schieck1997; the song of Bolivian Recurvebill can certainly be detected at distances > 50 m; authors’ pers. obs.), we consider that 100 m of survey transect covered an effective horizontal survey area of 1 ha. Thus, total transect length in metres was divided by 100 to obtain the size of the entire survey area in hectares.
All observations of both species on Cordillera Mosetenes were marked on a detailed map drawn with the aid of aerial photographs and a GPS. After two survey weeks, SKH targeted gaps between observation locations of each species with song playback to detect additional territories and/or determine territory limits along the trail system. Special caution was exerted to minimize possible errors in territory limits resulting from the observation of unmarked individuals. Once a pair of either species was located on a given day, SKH walked to the nearest observation point or cluster of points considered to be assignable to a neighbouring territory of that species, followed by the use of song playback broadcast in all directions to elicit a response of the presumed territory holders. If a response to playback came from the direction of the previous encounter the experiment was considered inconclusive. This procedure was repeated daily for most territories during the last 10 days of the survey.
Los Volcanes was initially surveyed by SKH in 1997 as outlined above. From June 2003 to November 2005 birds were monitored monthly by SKH and VHGS using constant effort mist netting, point counts and territory mapping on and in the vicinity of three permanent 1-ha plots at 1,050–1,200 m. Natural history data from this study on Bolivian Recurvebill are presented in the Supplementary materials.
Range size (extent of occurrence) estimates
In a recent study determining conservation priorities on the east Andean slope of Peru and northern Bolivia (Young Reference Young2007), the extent of occurrence of Bolivian Recurvebill and Yungas Antwren were estimated quantitatively for the first time by GIS-based predictive distribution modelling. Using the inductive model Maxent (Phillips et al. Reference Phillips, Anderson and Schapire2006; see also Hernandez et al. Reference Hernandez, Graham, Master and Albert2006) the extent of occurrence of each species was projected based on all known locality records as well as altitude, climate and vegetation data, including current habitat availability derived from Moderate Resolution Imaging Spectroradiometer (MODIS) data (Hernandez Reference Hernandez and Young2007). For each species four models varying in the use of the MODIS data were run (no MODIS data, MODIS data unsummarised, summarised by 2 km, summarised by 5 km). To evaluate the models, data could not be partitioned into training and evaluation records because of the scarcity and low spatial precision of available locality data. In this situation, review by specialists familiar with the species is often the best method available to determine the modelling procedure that produces the most realistic range prediction (Hernandez et al. Reference Hernandez, Franke, Herzog, Pacheco, Paniagua, Quintana, Soto, Swenson, Tovar, Valqui, Vargas and Young2008). Thus, SKH reviewed the output, determining whether any of the Maxent models produced reasonable results, and if they did, identifying the model and threshold (from the 0–1 scale Maxent output depicting how well the variables in each pixel match those found where the species has been recorded) that produced the most reasonable map for the species according to our present understanding of its distribution and habitat availability. Predicted areas of distribution where the species is known not to occur were eliminated. The final distribution maps are available at www.natureserve.org/aboutUs/latinamerica/maps_birds.jsp.
Results
Distribution, natural history and vocalizations
Bolivian Recurvebill and Yungas Antwren are now known from a total of 21 and 25 (27 when including two vagrant records) localities, respectively, which are fairly evenly distributed along the east Andean slope and extend across a latitudinal range from about 14°S to 18°S (Table 1, Figures 1 and 2). Details on records obtained by us and other ornithologists since 1995 are given in the Supplementary materials. Perhaps the most noteworthy of our observations are the first records (sound-recordings) of both species for Peru, obtained by SKH and VHG in 2005 and 2006 at Palmerani-Urubamba (Table 1) in extreme southeast depto. Puno, less than 3 km from the Bolivian border (see Supplementary materials). Prompted by the discovery of Bolivian Recurvebill at this site, a team from the Louisiana State University Museum of Natural Science visited the general area in 2007 and obtained the first Peruvian specimens of both species (D. F. Lane and A. Cuervo, pers. comm.; Table 1). Detailed information on the natural history and vocalizations of both species are given in the Supplementary materials.
Locality records (dark grey dots) of Bolivian Recurvebill Simoxenops striatus in Bolivia (LP = depto. La Paz, BE = depto. Beni, CO = depto. Cochabamba, SC = depto. Santa Cruz) and extreme southeast Peru (PU = depto. Puno). Light grey shading denotes areas within the main altitudinal range of the species (640–1,500 m). Numbers correspond to the following localities or locality clusters: 1 = Curva Alegre, Palmerani-Urubamba, Río Cocos; 2 = Serranía Eslabón; 3 = San Miguel Chico; 4 = Cerro Asunta Pata; 5 = Serranía Beu; 6 = Serranía Cuchilla; 7 = Illampu; 8 = Santa Ana; 9 = Mosetén Communal Lands, Río Ipiri; 10 = Laguna Carachupa; 11 = 48 km by road southwest of Villa Tunari, El Palmar, Alto Palmar, Serranía de Callejas; 12 = Río Saguayo; 13 = Serranía La Luna; 14 = Río Salado, Los Volcanes.
Locality records (dark grey dots) of Yungas Antwren Myrmotherula grisea in Bolivia (LP = depto. La Paz, BE = depto. Beni, CO = depto. Cochabamba, SC = depto. Santa Cruz) and extreme southeast Peru (PU = depto. Puno). Light grey shading denotes areas within the main altitudinal range of the species (600–1,400 m). Numbers correspond to the following localities or locality clusters: 1 = Curva Alegre, Palmerani-Urubamba, Río Cocos, Putina Puncu; 2 = Serranía Eslabón; 3 = Tuichi drainage: Hacienda Ubito, Río Machariapo, Yarimita; 4 = Cerro Asunta Pata; 5 = Serranía Pilón; 6 = Río Beni N Puerto Linares; 7 = Padilla; 8 = Serranía Bellavista, Caranavi; 9 = Santa Ana; 10 = Río Ipiri; 11 = Laguna Carachupa; 12 = Río Altamachi; 13 = El Palmar, Alto Palmar; 14 = Río Saguayo; 15 = Cerro Hosane; 16 = Río Macuñucú; 17 = Santa Rita; 18 = Los Volcanes, Serranía Raigones.
Range size (extent of occurrence) estimates
GIS-based predictive distribution modelling produced extent of occurrence estimates of 37,130 km2 for Bolivian Recurvebill and of 29,755 km2 for Yungas Antwren (Young Reference Young2007).
Population density and population size estimates
Along the trail system on Cordillera Mosetenes, covering an effective survey area of 20 ha, SKH determined eight Bolivian Recurvebill and six Yungas Antwren territories using territory mapping and song playback. Under the conservative assumption that only 50% of the average territory area was contained in the survey area and that a territory is occupied by two adult birds, extrapolated breeding population densities for the Laguna Carachupa area are 20 Bolivian Recurvebill and 15 Yungas Antwren pairs km−2. When further assuming that at least two thirds of the area of Cordillera Mosetenes (c. 2,000 km2, see Study area above), excluding areas above the altitudinal range of both species and marginal areas such as the northwestern tip with apparently suboptimal habitat, sustain those population densities, the overall breeding populations on Cordillera Mosetenes consist of about 80,000 Bolivian Recurvebills and 60,000 Yungas Antwrens. Taking into account a conservative error margin of 25%, those values are reduced to a minimum of 60,000 and 45,000 breeding birds, respectively. However, given the potential problems of territory mapping with unmarked individuals (primarily the potential overestimation of the number of territories by the false assignment of the same individual to more than one territory), and the extrapolation from a small study area of 0.2 km2 to an entire mountain range, a cautious interpretation of these values is recommended.
Although we lack similar quantitative data from other areas, it seems safe to conclude that neither species reaches such high densities at most of its other localities. The Río Cocos site (Table 1), however, an area with moderately abundant Guadua bamboo, might be an exception for Bolivian Recurvebill. Here, SKH and VHGS evaluated the density of the species somewhat less rigorously. Due to time constraints we made no specific effort to map territories, but we recorded what appeared to be six Bolivian Recurvebill territories in an effective survey area of c. 45 ha. Although this estimate is not directly comparable to that from Cordillera Mosetenes, given the larger survey area and shorter survey duration at the Río Cocos (see Supplementary materials), similar population densities at both sites seem plausible.
Discussion
Distribution
Bolivian Recurvebill and Yungas Antwren are now known from over 20 localities each (Table 1), which are distributed much more continuously than previously thought throughout Andean foothills and lower Yungas from depto. Puno in extreme southeast Peru to western depto. Santa Cruz in Bolivia (Figures 1, 2). In addition, the majority of localities of both species are inside or on the border of protected areas (Table 1). Their respective altitudinal distributions are also rather similar. That of Bolivian Recurvebill ranges from 640 m to mostly 1,500 m, locally extending up to 1,700 m in depto. La Paz (Table 1), but perhaps only under special local ecoclimatic conditions in somewhat sheltered valleys that have higher levels of solar insolation than outer Yungas slopes under direct impact from incoming clouds (see Herzog et al. Reference Herzog, Fjeldså, Kessler and Balderrama1999). Yungas Antwren occurs mostly from 600 m to 1,400 m, but extends locally up to 1,550 m in depto. La Paz; only at the extreme southern end of its range does it occur at altitudes as low as 450-500 m (Río Macuñucú, Santa Rita; Table 1), presumably due to the absence of lowland congeners from these areas (SKH, pers. obs.). The relative scarcity of records from large parts of depto. Cochabamba (Figures 1, 2) is probably mostly due to the difficult access to appropriate altitudes.
Both species might nonetheless be distributed somewhat patchily in at least parts of their range as some studies in seemingly suitable habitat did not record either species. Such areas include Río Leche (R. MacLeod, in litt.) and Cerro Leñe (SKH, unpubl. data, but see Herzog and Kessler Reference Herzog and Kessler1998) in eastern depto. Cochabamba, Serranías Sadiri, Tequeje and del Tigre in depto. La Paz (Madidi National Park; Hennessey Reference Hennessey2003b) and Serranía Bala in depto. Beni (Hennessey et al. Reference Hennessey, Herzog, Kessler and Robison2003a). Serranías Sadiri, Tequeje, del Tigre and Bala are the first foothill ridges in the northern Bolivian Andes that peak at about 900–1,000 m. Although they fall within the altitudinal range of Bolivian Recurvebill and Yungas Antwren, the suitable altitudinal amplitude of only about 300–350 m may be too narrow to sustain viable populations. The notion of a somewhat patchy distribution is further supported by the fact that, although both species inhabit an almost identical geographical range and a very similar altitudinal range, only 12 (33%) of the 36 localities in Table 1 were found to hold both species, which may be related to differences in (micro)habitat use between the two species.
Habitat associations
Parker et al. (Reference Parker, Stotz, Fitzpatrick, Stotz, Fitzpatrick, Parker and Moskovits1996) considered Bolivian Recurvebill as having high sensitivity to disturbance. We disagree and suggest classifying the species as having medium sensitivity to disturbance. Although not at high densities, Bolivian Recurvebill has been found in human disturbed habitats at Palmerani, 40 km southwest of Villa Tunari (S. Kreft, pers. comm.) and at the edge of logging gaps at Río Ipriri (see Supplementary materials). At Laguna Carachupa on Cordillera Mosetenes the dominant vegetation type was regenerating forest of variable age (often with stands of Guadua bamboo) caused by natural disturbances due to landslides or tree falls.
The statement of Ridgely and Tudor (Reference Ridgely and Tudor1994) that Bolivian Recurvebill apparently shows no preference for bamboo, which was also implied by Parker et al. Reference Parker, Bates and Cox1992 and based on the very limited data available at the time, needs to be revised. The fact that it reaches its highest known population densities in areas where Guadua bamboo is common to abundant (Cordillera Mosetenes, Río Cocos) combined with repeated observations of specialised foraging behaviour on Guadua bamboo (see Supplementary materials) are circumstantial evidence for a strong bamboo preference. However, the species is not an obligate bamboo specialist and persists at often much lower densities in humid and semi-deciduous forest without Guadua bamboo, where it forages in dense understorey or vine tangles, often near tree fall gaps. As observed by SKH at Los Volcanes (see Supplementary materials), it appears to employ similar foraging manoeuvres in these micro-habitats as it does in bamboo stands.
Yungas Antwren was thought to inhabit the mid-storey by Ridgely and Tudor (Reference Ridgely and Tudor1994), whereas Zimmer and Isler (Reference Zimmer, Isler, del Hoyo, Elliott and Christie2003) considered it a species of mid-storey and subcanopy that descends to the understorey only at forest edge. Data presented here (see Supplementary materials) indicate that Yungas Antwren, like its closest relatives Plain-winged Antwren M. behni, Unicoloured Antwren M. unicolor and Alagoas Antwren M. snowi (the ‘plain-winged group’; Whitney Reference Whitney1994, Whitney and Pacheco Reference Whitney and Pacheco1997, Zimmer and Isler Reference Zimmer, Isler, del Hoyo, Elliott and Christie2003), is an understorey species that moves up to mid-level or subcanopy only occasionally while foraging with mixed-species flocks. Its regular occurrence in semi-deciduous forest in depto. La Paz (Perry et al. Reference Perry, Kessler and Helme1997, this study) also is a rather recent discovery. The presence of typical humid forest species in semi-deciduous and deciduous forest of isolated rain-shadowed valleys embedded in the humid Bolivian Yungas is a general pattern that has only recently been documented to its full extent (Herzog and Kessler Reference Herzog and Kessler2002, Reference Herzog and Kessler2006). Nonetheless, the first record of Yungas Antwren from semi-deciduous forest originated from Santa Rita (Remsen et al. Reference Remsen, Parker and Ridgely1982; Table 1), depto. Santa Cruz, which went unnoticed due to the erroneous assignment of coordinates to this locality (see footnote 2 in Table 1). T. A. Parker's observation of several individuals on Serranía Raigones, which was mentioned only ‘in passing’ by Collar et al. (Reference Collar, Gonzaga, Krabbe, Madroño Nieto, Naranjo, Parker and Wege1992), originated from a deciduous forest area where semi-deciduous forest is restricted to narrow gullies (SKH, pers. obs.) at the extreme southern end of the species’ range. However, as with nearby Los Volcanes, we consider it unlikely that Serranía Raigones holds a breeding population of Yungas Antwren. Rather, these observations may be related to source-sink dynamics, where individuals from the core, evergreen areas spill into suboptimal deciduous habitat.
Range size and population size
The global extent of occurrence was previously estimated at 19,900 km2 for Bolivian Recurvebill and 32,000 km2 for Yungas Antwren (BirdLife International 2000, 2004, 2007a,b). The most recent estimates obtained by GIS-based predictive distribution modelling (Young Reference Young2007) projected a rather similar value of 29,755 km2 for Yungas Antwren, but a notably greater extent of occurrence of 37,130 km2 for Bolivian Recurvebill, which is almost twice as large as that estimated previously. These new estimates thus reconfirm the classification of both species as restricted-range species (see Stattersfield et al. Reference Stattersfield, Crosby, Long and Wege1998).
The population size of Bolivian Recurvebill and Yungas Antwren was previously thought to be between 2,500 and 10,000 mature individuals (BirdLife International 2004, 2007a,b). Our density estimates from Cordillera Mosetenes indicate that this area alone holds breeding populations of both species of well in excess of 10,000 individuals. Although total population sizes are difficult to estimate due to a lack of quantitative data from other localities, we consider that the global population of both species must number on the order of several tens of thousands of mature individuals. Cordillera Mosetenes seems to be the stronghold for both species, probably due to its high habitat heterogeneity with much natural disturbance and, for Bolivian Recurvebill, the abundance of thick-stemmed Guadua bamboo.
Conservation status
Bolivian Recurvebill and Yungas Antwren are currently considered ‘Vulnerable’ (BirdLife International 2007a,b). The latter species is listed based only on IUCN criterion C2a (BirdLife International 2007a), i.e. its population is estimated to number fewer than 10,000 mature individuals and a continuing decline in numbers of mature individuals is observed, projected, or inferred, with no subpopulation estimated to contain more than 1,000 mature individuals. Our density estimates from Cordillera Mosetenes, combined with the new locality records, indicate that the global population size of Yungas Antwren is much greater than 10,000 mature individuals, that the Cordillera Mosetenes subpopulation is much greater than 1,000 mature individuals and that the global population is much less fragmented than previously thought. Criterion C2a thus does not apply to Yungas Antwren.
Bolivian Recurvebill also is listed under criterion C2a (BirdLife International 2007b), and as with Yungas Antwren, our data strongly suggest that this criterion does not apply to the species. Additional criteria that are thought to apply to Bolivian Recurvebill are B1a+b (BirdLife International 2007b), which estimate the species’ extent of occurrence to be less than 20,000 km2, combined with no more than 10 known localities and a continuing population decline being observed, inferred or projected. The numerous new localities presented above combined with the new extent of occurrence estimate of 37,130 km2 (Young Reference Young2007) document that criteria B1a+b also do not apply to Bolivian Recurvebill.
In conclusion, none of the IUCN criteria currently used to assign ‘Vulnerable’ status to both species (BirdLife International 2007a,b) actually apply, and we recommend that Bolivian Recurvebill and Yungas Antwren be downlisted to ‘Near Threatened’. Although no direct evidence for a population decline exists, given their small range it remains a valid threat to both species due to high levels of habitat conversion in the Andean foothills and lower Yungas of Bolivia. Further, even though there remains no doubt that both species have a global population size of well above 10,000 mature individuals, our estimates of > 50,000 individuals are essentially based on a single locality, and confirmation of our density estimates from additional localities on Cordillera Mosetenes are desirable. Both species have been recorded in several protected areas, but most Bolivian national parks offer little real protection to their threatened species because areas such as Amboró National Park often suffer locally from illegal invasions and forest clearing by subsistence farmers (e.g., Bayá Reference Bayá2006). In addition, under current Bolivian legislation, the exploitation of natural resources has priority over the preservation of protected areas and there remains the risk that these areas could be seriously altered in future extractions of natural resources or road construction projects.
Other threatened Yungas species
Six bird species currently considered threatened occur in the humid forests of the Bolivian Yungas (excluding birds of treeline habitats and Polylepis woodlands such as Royal Cinclodes Cinclodes aricomae), and one might wonder if the conservation status of some of them should not also be re-evaluated in light of newly available data. Two are listed as ‘Endangered’ (Horned Curassow Pauxi unicornis, Yellow-rumped Antwren Terenura sharpei) and four as ‘Vulnerable’ (Military Macaw Ara militaris, Scimitar-winged Piha Lipaugus uropygialis, Green-capped Tanager Tangara meyerdeschauenseei, Cerulean Warbler Dendroica cerulea) (see www.birdlife.org/datazone/species/index.html).
The Nearctic-Neotropical migrant Cerulean Warbler reaches the southern terminus of its non-breeding range in northern Bolivia, where it is known from only a handful of records (see Tobias and Seddon Reference Tobias and Seddon2007), so virtually nothing can be said about its conservation status based on such data. The situation is similar for Green-capped Tanager, a species formerly considered as endemic to Peru and reported from a single Bolivian locality (Hennessey and Gomez Reference Hennessey and Gomez2003). The status of Scimitar-winged Piha was recently reviewed by Bryce et al. (Reference Bryce, Hennessey, MacLeod, Evans, Ewing, Herzog, Maccormick and Gomez2005), who recommended continued classification as ‘Vulnerable’. The widely distributed Military Macaw, on the other hand, does not appear to be highly threatened in Bolivia, where it is common throughout most of the Yungas of depto. La Paz and northern depto. Santa Cruz (rare to uncommon elsewhere in the Bolivian Andes; authors’ unpubl. data), and it is found rather infrequently in the local pet trade (Herrera and Hennessey Reference Herrera and Hennessey2007).
To the contrary, both ‘Endangered’ species, which are also restricted-range species (Stattersfield et al. Reference Stattersfield, Crosby, Long and Wege1998), are properly listed as such. Both seem to be naturally rare and are threatened by ongoing, widespread habitat conversion in the foothills and, in the case of Horned Curassow, a high sensitivity to hunting pressure (BirdLife International 2000). Bolivian records of Yellow-rumped Antwren are restricted to only three areas in deptos. La Paz and Cochabamba (Cerro Asunta Pata, Louisiana State University Museum of Natural Science specimen; Serranía Bellavista, Remsen et al. Reference Remsen, Parker and Ridgely1982, BirdLife International 2000; the Chapare region near San Onofre, Remsen Reference Remsen, Parker and Ridgely1982, Brumfield and Maillard Reference Brumfield and Maillard2007), but the species no longer seems to occur on Serranía Bellavista (VHGS, unpubl. data) and has not been found at additional sites despite specific efforts (Hennessey Reference Hennessey2004, SKH and VHG, unpubl. data).
Acknowledgements
Thanks to S.W. Cardiff, A. Cuervo, S. Kreft, D.F. Lane, J.V. Remsen, N. Renaudin, N. Seddon, J.A. Tobias and B.M. Whitney for sharing their unpublished data; to N.H. Rice and K. Zyskowski for information on the whereabouts of Bolivian Recurvebill specimens; to I. Gómez for information on Colección Boliviana de Fauna specimens; and to R. MacLeod, S. Marsden, B.M. Whitney and an anonymous reviewer for comments on an earlier draft of the manuscript. We are grateful to the Bolivian Protected Areas Service (SERNAP) for permission to work in several national parks. M. Fernández, L. Pyritz, R. Soto and D. Soux assisted with mist-netting and ringing in Los Volcanes. SKH's field work was supported by the German Research Council (Deutsche Forschungsgemeinschaft), the German Academic Exchange Service and the Gesellschaft für Tropenornithologie. ABH is grateful for the research opportunities provided by Veterinarians without Borders in Pilón Lajas Biosphere Reserve and by the Living Landscapes Program of the Wildlife Conservation Society (WCS) in Madidi National Park, financed by USAID/Global and WCS International through cooperative agreement LAG-A-00-99-00047-00, and additional support from the Gordon and Betty Moore Foundation for the WCS Conserving Landscapes in Amazonia program. The opinions expressed are those of the author and do not necessarily reflect USAID criteria. Field work of MK was supported by the German Research Council. Funds for work at the Altamachi River were obtained by R. MacLeod and A. Maccormick (see MacLeod et al. Reference MacLeod, Ewing, Herzog, Bryce, Evans and Maccormick2005 for a list of funders). The expedition to Laguna Carachupa was made possible by financial support from the Conservation, Research and Exploration Fund of the National Geographic Society, the German Research Council, the Weeden Foundation, BIOPAT and the A.F.W.-Schimper Foundation. The expedition to the confluence of the Santa Elena and Ipiri rivers formed part of the Bolivian Important Biodiversity Areas project of R. MacLeod and A. Maccormick and was supported by the Darwin Initiative Scheme and Conservation International. The expedition to the Río Cocos was funded by the Migratory Bird Program of The Nature Conservancy (D. Mehlman). The support and facilities afforded by Asociación Armonía's Bird Conservation Centre, Bolivian Bird Database and the David Snow Library was invaluable. The Cornell Laboratory of Ornithology's Macaulay Library of Natural Sounds provided equipment loans, tapes and archival assistance to ABH.
